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Bird communities in small woods in an agricultural landscape: Effects of area and isolation
Biological Conservation 34 (1985) 333-352
Bird Communities in Small Woods in an Agricultural Landscape: Effects of Area and Isolation P. O p d a m , G. Rijsdijk & F. Hustings Research Institute for Nature Management, PO Box 46, 3956 ZR Leersum, The Netherlands
ABSTRACT The distribution oJ breeding bird species in 68 small woodlots in two areas o] agricultural landscape was investigated. Effects oj area, habitat variation, interpatch distance, and distance j?om extensive woods were analysed with the help oJ multivariate techniques. No correlation was Jound between number of breeding bird species and isolation variables, but the degree of isolation was shown to affect the number oJ bird species restricted to mature woods. Species showed different responses to changes ojarea or isolation variables. It is concluded that,Jor several species of woodland birds, patches of mature woodland can be regarded as habitat islands. Some indications are given to apply the regression modelsjound to landscape planning.
INTRODUCTION The distribution of birds in a patchy environment is determined primarily by the presence of suitable habitat. The size of the habitat patches may, however, affect the presence of species, since patch size is related to population size and thereby to extinction rate (Jones & Diamond, 1976; Wright & Hubbell, 1983). At the same time, the distance between the patches may be inversely related to the frequency of interpatch dispersal (Whitcomb et al., 1981; Opdam, 1983; Lynch & Whigham, 1984). The equilibrium theory of MacArthur & Wilson (1967) combined extinction and immigration rates in a dynamic model for the number of species on oceanic islands, and various authors later extended the 333 Biol. Conserv. 0006-3207/85/$03.30 ,t~ ElsevierApplied SciencePublishersLtd, England, 1985. Printed in Great Britain
334
P. Opdam, G. Rijsdiik, F. Hustings
predictions of the model to habitat patches on the mainland. The empirical support for this theory and the implications for reserve design have been discussed exhaustively (Diamond, 1975; Connor & McCoy, 1979; Gilbert, 1980; Margules et al., 1982). However, evidence supporting an area-dependent extinction rate and a distance-dependent immigration rate is scanty (Gilbert, 1980; Margules et al., 1982). For mobile species, such as most birds, Margules et al. (1982) and Ambuel & Temple (1983) even postulate that isolation of reserves will not affect local immigration. In this paper the distribution of breeding birds is discussed in relation to the size and degree of isolation of wooded patches. It is clear that in the modern cultivated landscape, patches of habitat tend to decrease in size and become more and more widely separated from each other. Quantification of the relation between landscape structure and the distribution and survival of fauna groups is an important task for nature conservationists. We chose birds for the present analysis because they can be censused quickly, and woods because great numbers of birds breed in this type of habitat. Effects of patch size on the number of breeding-bird species have been studied often, but in most of these studies, the effects of size p e r se were not separated from those of habitat diversity increasing with size (Connor & McCoy, 1979, but see Ambuel & Temple, 1983). Furthermore, in most studies the variable "number of species" encompassed all the species of a taxonomic order. However, the study done by Humphreys & Kitchener (1982) indicated, as expected, that species restricted to habitats in isolated patches may show species area relations differing strongly from those of species that use adjacent habitats as well, and Galli et al. (1976), Whitcomb et al. (1981) and Opdam & Retel Helmrich (1984) have also pointed to species-specific relations with patch size. The impact of isolation on birds in habitat patches is not quite clear. An effect has been claimed by Fritz (1979), Whitcomb et al. (1981) and Opdam et al. (1984). In the first-mentioned study the spruce grouse C a n a c h i t e s canadensis was shown to occupy habitat remnants more often the closer these patches were to another patch. In the other studies, large sets of data were used to analyse the island effect of small woods on the number of breeding birds. However, the results of Whitcomb et al. (1981) were not unambiguous because in their data wood area and degree of isolation were strongly interdependant, whereas Opdam et al. (1984) could not account for possible habitat variation affecting the distribution
Small woods as habitat islands".[or breeding birds
335
of bird species. In a study on bird-species numbers in British woods, Helliwell (1976) found no effect of isolation, probfibly because he had included in the analysis too m a n y species for which the woods did not represent isolated habitat patches. In Vuilleumier's (1970) analysis of birds on mountain tops the number of species was even positively correlated with distance, but after re-examination of the data Mauriello & Roskoski (1974) claimed that the coefficient of distance should have been negative. The results of the studies done so far are not very convincing, the more so because differences between species were not quantified. In a recent paper, however, Lynch & Whigham (1984) presented an excellent analysis of the avian communities of 185 forest patches ranging in size from 5 to more than 1000 ha and divided over two regions. They could demonstrate the impact of isolation on the distribution of most of the species they studied. In our study we followed more or less the same strategy and selected in an agricultural landscape 68 small woodlots, ranging in size from less than 1 ha to 20 ha. The woodlots differed substantially as to degree of isolation, but otherwise we tried to keep habitat characteristics as uniform as possible. The remaining habitat variation was measured. The presence of all breeding bird species was determined and the following predictions were tested: (a)
Woodlot size and degree of isolation affect the number of bird species. (b) Species that are restricted to woods occur less often in small woodlots than in large ones, even after corrections for differences in habitat structure. (c) These species are absent most often in the most isolated woodlots. (d) Species differ as to the degree to which they are affected by area and isolation. METHODS Two study areas were chosen (Fig. 1). One of them, the Gelderse Vallei (Fig. l a), an agricultural area of about 400 km 2 in the central part of The Netherlands, is surrounded on three sides by extensive mixed forests. Many woods, wooded banks, hedgerows and small groups of trees are scattered over the area, but most of the woods are coppice or half-grown. Within this area 40 mature deciduous woods were selected. The second
336
P. Opdam, G. Rijsdijk, F. Hustings
/ / /
o
,/ /
/ /
o &
o
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• 0
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sample plots • 0-2, 0ha zx 2, I - 6 , 0 h a o >6, Oha
Fig. I.
--*-- dutch border ~-~
forest
Location of sample sites in (a) the Gelderse Vallei area and (b) the southern part
of the province of Limburg (Zuid Limburg), showing the outline of surrounding forests. (Scale: 1 cm equals 22km).
area is situated in the southernmost part of the province of Limburg and extends over 200 km z. On the north and south, extensive mixed forests border the area. In this agriculturally-used landscape deciduous woods are scattered; among these 28 mature woods were suitable for our study. The Limburg area (Fig. l b) is more open than the Gelderse Vallei, with fewer wooded sites and groups of trees between the selected woods. Although the sampling plots were selected for uniformity of the tree layer, some divergence between the sites had to be accepted. Moreover, the coverage, structural heterogeneity, and species composition of the shrub layer varied considerably. Therefore, habitat diversity variables were recorded in the field (Table 1). Most edges of the woodlots were sharp changes from trees to cultivated fields. From maps 1:25 000, isolation variables were calculated, and a map 1:10 000 was used to estimate the area of the woodlots (Table I). Because oblong woods have a higher edge-to-interior ratio than compact woods and the forest-edge may represent a different habitat type, the woods were
Small woods as habitat islands jor breeding birds
337
TABLE 1
Variables for Habitat and Landscape Attributes Determined for Each Sample Site Habitat variables
Trunk CovH CovS StrDiv
Trunk diameter, a measure of age differences between trees (2 classes) Coverage of the herb layer (3 classes) Coverage of the shrub layer (3 classes) Structural diversity of tree and shrub layers (3 classes) Dominant tree species (9 types)
Variables of size and landscape
SW A TA DLF DW DAW NDW AAW WB
Shape of the woodlot (compact or oblong) Area of mature deciduous wood (in ha) Total area of wood containing the selected site Distance from large forest areas, measured as the shortest distance between the edge of the woodlot and the edge of an extensive forest area Distance from nearest mature deciduous wood larger than 20 ha (in km) Distance from nearest wood of any type larger than 20 ha (in km) Number of mature deciduous woods within a 3 km radius from the centre of the woodlot Area of wood of any type within a 3 km radius from the centre of the woodlot (in ha) Proximity of wooded banks or rows of mature trees
classified as o b l o n g or c o m p a c t . S o m e o f the w o o d l o t attributes a p p e a r e d to be c o r r e l a t e d (Table 2). E a c h w o o d l o t was visited five times, between M a r c h and the middle o f J u n e o f 1983, for periods o f 15 min each. D u r i n g each visit all parts o f the w o o d were scanned for birds showing b e h a v i o u r indicating the presence o f a territory. In the largest w o o d l o t s m o r e time was n e e d e d to cross the whole area, at m o s t between 30 and 45 min. F o r all species, the first relevant o b s e r v a t i o n was r e c o r d e d o n each visit a n d the presence o f a t e r r i t o r y was derived f r o m the c o m b i n e d visits on the basis o f the criteria in Hustings et al. (1985). F o r m o s t s e d e n t a r y species at least two o b s e r v a t i o n s m a d e o n separate visits were required, but for some species for which o b s e r v a t i o n efficiency was low we accepted a t e r r i t o r y on the basis o f o n l y one r e c o r d in the p o s t - m i g r a t i o n period. In this way a list o f b r e e d i n g birds was o b t a i n e d for each w o o d l o t . T h r e e sets o f analyses were carried out: (a) with the n u m b e r o f species restricted to w o o d s ; (b) with the n u m b e r o f species restricted to m a t u r e d e c i d u o u s w o o d s ; a n d (c) with the p r e s e n c e / a b s e n c e o f p a r t i c u l a r species. T h e last o f these variables assumes either 0 or 1, the o t h e r two range f r o m
P. Opdam, G. Rijsdo'k, F. Hustings
338
TABLE Significant
Correlations
between
Woodlot
2
Attributes
pertaining
to Area
and
Isolation
Gelderse Vallei A~ DAW
WB
5°Jo
--
TA
0 . 1 ~o
--
DLF
--
0.10/o
DW NDW
.
AAW
--
1 o/ /O
__
--
0 - 1 o/. /o
A
DAW
WB
TA
DLF
- -
.
. 5 o~
-_
_
.
0.1 ~o .
.
.
. __
__
DW
NDW
AAW
AAW
WB
Limburg A TA
0 . 1 ~o
DLF
--
DW
--
DAW
--
--
1 ~o
NDW
--
--
O' 1 ~o
--
--
AAW
- -
0 . 1 °/o
0 . 1 °.,o
1 ~o
WB
5 ~o
5 O;o
.
A
TA
DLF
a See Table
-1~o O . l ~o
.
. DW
1 ~o
. DAW
NDW
1.
7 to 39 and from 1 to 11, respectively. The variation of these variables in dependence of the other woodlot attributes was analysed by stepwise multiple linear regression using GENSTAT (Alvey et al., 1982). For several variables (e.g. size and most isolation variables) we assumed nonlinearity in their relation to species number and therefore applied logarithmically transformed values.
RESULTS All woodland species combined As a rule, in studies on the island effect island attributes are related to the total number of species on the (habitat) island, excluding species that also use the habitats surrounding the island. Likewise, we excluded those birds feeding mainly on surrounding agricultural land, and studied the island
Small woods as habitat islands JOt breeding birds
339
effect on the remaining species, which we called w o o d l o t species. Since these birds can inhabit different layers, i.e., the g r o u n d layer, the shrub layer, the c a n o p y , or a c o m b i n a t i o n of layers, some of t h e m are not restricted to the type of w o o d under study, but could also occur in nearby or even adjacent plantations, coppices, hedgerows, or gardens. A significant a m o u n t o f variation in the n u m b e r o f w o o d l o t species is explained by w o o d l o t area a n d a variable o f tree-layer diversity t h a t accounts for the c o m b i n a t i o n o f oaks and beeches (Table 3). This habitat variable was strongly correlated with o a k w o o d a n d the presence of large trees. At the 5 ~o level of significance, none of the isolation parameters were selected. Hence, for all species c o m b i n e d , an effect of isolation could not be d e m o n s t r a t e d . P r o b a b l y the isolation effect was too small to be measurable, because, for most of the species in the set, the w o o d s did n o t represent true habitat islands. W o o d l o t size might be partially related to h a b i t a t diversity, especially as to the coverage, structural heterogeneity, a n d species composition in the shrub layer. A l t h o u g h species area relations are generally described in a double TABLE 3
Summary of Stepwise Multiple Regression Analysis, Showing the Best Over All Fits for the Number of Bird Species in the Woodlots (Standard error between brackets) Sw~ = 16.56 + 2.42 In A + 2.53 BO (0-95) (0"75) (1.22) SwL= 19.96 + 5.161n A - 9.27 POP SMG=5"24--0-551n DLF+0.871nA+I.30BO (0.48) (0-20) (0.31) (0-51) S m = 6.00 + 1.611n A - 0.85 D L F - 2.69 P O P - 1.37 BIO (0-33) (0-16) (0.22) (1.06)' (0"63) SM~=4.11+0-96BO+0.941nA-0.731nDNF+I.85WB Sw, All woodlot species S M, Species of mature deciduous woods G, Gelderse Vallei L, Limburg A, Area BIO, birch-oakwood BO, beech-oakwood POP, poplar-alder DLF, Distance from large forest DNF, Distance from the nearest forest larger than 20 ha
V2 = 39.3 R2 = 42.3 V2 = 78.1 R2 = 79-8 Vz=47.2 R2=51.2 V2 = 86.5 R2 = 88.5 V-'=55.3
R2=61.0
340
P. Opdam, G. R(jsdijk, F. Hustings
logarithmic form, we preferred a semi-logarithmic form because the regression on S gave a slightly better fit (R 2 - - 2 9 . 2 against 27.5). Species restricted to mature woods Since we selected mature deciduous woods as habitat islands, isolation might be particularly relevant with respect to species restricted to woodlots of this type. Therefore a selection was made of 15 species that are found as breeding birds particularly in mature woods, at least in the areas under study (Table 4). Most of these species are numerous in the extensive forests surrounding the study areas. The effects of woodlot size and isolation on the number of these species (S ~ were assessed in the two areas separately. The results of the regression analysis (Table 3) show that in both areas woodlot size and distance to a large forest are significantly correlated with species number. Additionally, the regressions included variables for habitat differences. In the Gelderse Vallei beech-oakwood contained more species than pure oak stands, presumably because TABLE 4 Occurrence of Bird Species of Mature Deciduous Woods in the 68 Plots. (Values are numbers of plots in which each species was
recorded) Species
Values
Black woodpecker Drvocopus martius Woodwarbler Phylloscopus sibilatrix Redstart Phoenicurus phoenicurus Golden oriole Oriol,~s oriolus Green woodpecker Picus viridus Pied flycatcher Ficedula hypoleuca Hawfinch Coccothraustes coccothraustes Lesser spotted woodpecker Dendrocopos minor Marsh tit Parus palustris Nuthatch Sitta europaea Great spotted woodpecker Dendrocopos major Spotted flycatcher Muscicapa striata Tree creeper Certhia brachydactyla Blue tit Parus caeruleus Chaffinch Fringilla coelebs
2° 4b 4 5 7 8" 12b 15 ' 29 37 40 54 59 66 66
In the Gelderse Vallei only b In Limburg only
Small woods as habitat islands for breeding birds
341
beeches offer more nesting holes. In the Limburg area two types of wood (poplar-alder and oak-birch) had fewer species than oakwood and beech-oakwood. These types of wood had mainly half-grown trees and presumably offered fewer feeding sites for bark-feeding birds and fewer nesting holes. Again, because of the better fit, we used a linear-dependent rather than a logarithmic-dependent variable. The variable distance to large forest in the Gelderse Vallei regression model could be replaced by a combination of three variables. The total amount of variation accounted for by this more complicated model did not differ much from that with the simple one. Two of these variables are regarded as indicators of isolation (presence of tree rows and wooded banks around the woodlot and amount of woods within a 3 km radius). Shape of wood, the third variable, is considered as a habitat variable. Oblong-shaped woods, which contained fewer species, are affected most by the surrounding environment (e.g. microclimate) and may therefore be less suitable for typical woodland birds. The coefficients of woodlot size did not differ significantly (t-test, t = 1.17) between the two areas. The greater amount of variation explained by this variable in the Limburg area is attributed to its greater range compared to the Gelderse Vallei (Fig. 2). Since the sample of wooded sites was selected on the basis of tree-layer homogeneity, habitat diversity is rather small. None of the habitat variables was correlated with woodlot size. Hence we suggest that most, if not all, of the effect ofwoodlot size is due to the mere effect of area as such. • L i m b u r g : S : 4 , 7 2 ÷ I , 7 2 In A • G e l d e r s e V a l l e i : S=4,57÷1,27 In A
S 20 16
12 •
04-
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•
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-2(0.14ha)
-I(037ha)
I
(1.00ha} I(2,72ha) 2(7.39ha)
I
3'(20.09ha1 4 InA
Fig. 2.
Species-area plot of the two study areas. (Scale: 1 cm equals 22kin).
342
P. Opdam, G. Rijsd(jk, F. Hustings
Distance to large forest has a somewhat greater impact in the Limburg area as compared with the Gelderse Vallei. This isolation variable ranged between 0.1 and 6.5 km in Limburg and between 0.1 and 9.8 km in the Gelderse Vallei. Calculated over the maximal range, the number of bird species diminished from 8 to 4.4 and from 6.5 to 4, respectively, all other variables being constant. However, the difference between the regression coefficients is not statistically significant (t-test, t = 1.01). A difference between the two areas might be due to the greater amount of woodland and rows or groups of trees in the Gelderse Vallei, which might increase the dispersal rate of woodland birds. We conclude that distance from large forest area is a significant factor determining the distribution of birds inhabiting mature deciduous woods.
Analysis of separate species Thus far, the number of species has been used to analyse the island effect in isolated woodlots. The underlying assumption was that all species are equal with respect to the relationship between woodlot area, population size, and extinction rate, as well as the extent to which their dispersal is hampered by interpatch distance. However, differences between species are plausible and may give more insight into the mechanism leading to the observed species-area relations. Therefore, we undertook an analysis at the species level. For this purpose, we used the presence/absence of a species in the woodlots as a dependent variable in logistic regression analysis. This meant, however, that the amount of variation became much smaller, especially for species occurring either in a very few or in almost all woodlots. The best possible solution to this problem was to combine all woodlots, which was acceptable because of the small differences between the two regions as to the effects of area and isolation. The occurrence of the species in the woodlots is shown in Table 4. Species found in less that 10 ~o or more than 90 ~o of the samples were omitted from further analysis. The regression analysis was restricted to simple models, each containing one variable for size of the woodlot, one isolation variable and two habitat variables (oak-beech type and other woodland types). We also added a region variable (a d u m m y variable) to account for possible differences between the two areas under study. Three sets of regressions were run, each with a different isolation variable, namely distance from large forest, amount of woodland within 3 k m radius, and proximity of wooded banks or rows of trees.
Small woods as habitat islands for breeding birds
343
For most of the species none of the habitat variables explained a significant part of the variation, with the exception of the nuthatch and the great spotted woodpecker, which occurred more often in beech oak woodland than in any of the other types. The coefficients for woodlot size are shown in Table 5. The ranking of the species according to these coefficients in the three sets of regressions remains roughly the same, especially if only significant coefficients are considered. This concordance can be seen as support for the reliability of these results. TABLE 5 Area Effect in Woodland Birds (Coefficients of correlation between frequency of occurrence and woodlot size, allowing for isolation and habitat differences. Only significant coefficients (P <0.10) are given. The coefficients were calculated for three sets, using as an isolation measure area of woodland within 3 km radius (1), distance from large wood (2), and proximity of wooded banks and rows of trees (3).)
Species Great spotted woodpecker Tree creeper Redstart Nuthatch Hawfinch Marsh tit Lesser spotted woodpecker
(I) 2-28* 1.57" 2.11 1.10" 0.97* 0.87* 0.70
(2)
(3)
2.42* 1.62" 1.14 1.09" 0.93* 0.90* 0.69
2.21" 1.84" -0.99 1-92 1-02" 0.62
* P smaller than 0.05
The regression coefficients for the isolation variables are presented in Table 6, except for the proximity of wooded banks, which showed very low T values. The probability of occurrence of nuthatch and marsh tit is significantly affected by the two isolation variables used and that of the redstart by the amount of nearby forest only, whereas for the lesser spotted woodpecker the coefficient of this isolation variable was almost significant. The coefficients of the two variables show a positive correlation. A more detailed consideration of the relation between presence/absence of species and woodlot size may shed more light on the causal
N=11
0-I.0
/
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,--~
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,/
f/
/
-~
"''. pied flycatcher
lesser spotted woodpecker
~lreat
spotted woodpecker
/~_ spotted flycatcher
14
12
17
14
1.I'-2,0 2.1'-3.0 3.1'-6,0 >6.'0 size
~
chaffinch
~ k
(%) I00-
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,
//
///i
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/
N=11
14
12
17
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0"1.0 1.1'-20 2.1'-3.0 3,1'-6.0 "6.b size
hawf, nch
.- "''marsh tit*
nuthatch*
/ ~ " ~ - - - - ~ - b I ue tit*
/"2JL_/ /-
/
/
./
/ " // .~. . .. .
/
//
~t~,t ree creeper*
Fig. 3. Incidence curves showing the frequency of occurrence (in % of maximal frequency) according to five classes of wood size (in ha) of ten species restricted to mature deciduous woodland (Gelderse Vallei + Zuid Limburg). *Significantly differing from random distribution (X 2 test, P < 0.05).
50
100
(~)
Small woods as habitat islands for breeding birds
345
mechanism underlying the distribution patterns found. In Fig. 3 the woodlots have been classified according to five size classes, which were chosen such that the woods were more or less evenly distributed over the size classes. The blue tit and chaffinch are absent in only a few of the smallest woods. The incidence curve of the spotted flycatcher suggests an effect of habitat rather than of woodlot size. In the Gelderse Vallei this species was recorded more often in beech-oak woods than in oak woods. The great spotted woodpecker and tree creeper occur in almost all woods exceeding 3ha and 1 ha, respectively, but the woodpecker was not recorded in woodlots smaller than 1 ha. The stagnation in the upward trends in class 3 may be due to lack of suitable habitat. The nuthatch and marsh tit show no clear minimal habitat size: apparently they can live in even the smallest woodlots. Their absence in some of the woods must be due to lack of suitable habitat (cf. distribution of the great spotted woodpecker and tree creeper), to isolation or extinction. The distribution of the lesser spotted woodpecker is difficult to explain, except by referring to its very clumped distribution pattern in the Gelderse Vallei. The hawfinch was not recorded in the Gelderse Vallei woods, though it occurs in considerable numbers in the surrounding extensive forests of the Veluwe and the Utrechtse Heuvelrug. In the remaining woods the distribution is partially explained by an effect of woodlot size. The pied flycatcher is too scarce to draw reliable conclusions from its incidence curve. We conclude that at the species level there is a good evidence for effects ofwoodlot size, especially in the great spotted woodpecker (minimal area) and in the tree creeper, nuthatch, marsh tit, and hawfinch. Isolation of woodlots is a significant factor in the distribution of the nuthatch, marsh tit and probably the redstart and lesser spotted woodpecker. Because the species are affected to different degrees, they show species-specific distribution patterns.
DISCUSSION Evaluation of the bird survey method
Some researchers have been concerned about the influence of sampling methods on species-area relationships. Woolhouse (1983) argued that sampling time per unit area must be constant for all sites surveyed. For a
346
P. Opdam, G. Rijsdijk, F. Hustings
qualitative survey of breeding-bird territories, this would mean for each wood and for each bird species, equal time spent in one territory. Because the position of territories cannot be known in advance, this condition is hardly attainable in practice, if at all. Further problems are associated with the differences in territory size and observing chance between the species and from the fact that isolated territory owners in a small woodlot may be less active in territorial display than birds in territories surrounded by neighbours. Also, one territory out of a cluster of several is more likely to be recorded solely by pure chance than an isolated one is, even if the sampling effort is the same. We attempted to deal with these problems in several ways. In the first place, observation time was held constant in the smallest woods (up to 4-5 ha, depending on the shape). These woods were so small that it was highly probable that any bird singing would be noticed. In the larger woodlots, which were less easy to survey at a glance, observation time was increased, up to 45 min for a 30 ha wood, depending on the time needed to take a quick look at every section of the wood. Thus, sampling effort (time per unit area) was highest in the smallest woodlots, in agreement with the decreased territorial activities of isolated birds and the increasing chance of recording a single specimen with increasing population size. With this method, however, single small territories in large woods were underestimated, and therefore differences between small and large woods may be somewhat underrated. Because in large woods most of the species in question were represented by several breeding pairs, this bias is assumed to be very small. Differences in recording chance between species were accounted for by the species-specific criteria for the number of records (in combination with recording date) required for the acceptance of a territory (Hustings et al., 1985). These criteria were chosen such that all species were surveyed at an accuracy level of at least 90 ~ (Kwak & Meijer, 1985). The role of patch size
Lynch & Whigham (1984) concluded that the occurrence of many species can be predicted better from structural and floristic characteristics of woods than from patch size and isolation. However, in the uniform series of woods we have intentionally chosen, habitat differences play a minor role and the distribution of most bird species, as well as the composition of avian communities, are predicted best from patch size. The incidence
Small woods as habitat islands Jbr breeding birds
347
curves (Fig. 3) indicate that with increasing woodlot size species are added in a fairly predictable sequence. Several explanations can be offered for this pattern: (1) The bird community in a wood is a random sample of that in the nearest larger woods, and with increasing patch size species are added in order of their overall abundance. Species do not differ as to immigration or extinction rate. This 'random sampling hypothesis' does not imply any biological process and can be used as a null hypothesis to test alternative models (Connor & McCoy, 1979). (2) Forest-interior species cannot persist in the smallest woods because of competition with edge species for nest sites or for food, or become extinct as a result of predation by predators from the surrounding landscape (Ambuel & Temple, 1983). (3) In the smallest woods, populations have the highest extinction rates due to stochastic perturbations of the population number (MacArthur & Wilson, 1967). (4) Species differ as to the minimal critical area they need to satisfy their food requirements during the breeding season. The random-sampling hypothesis predicts that the slopes of the incidence curves are equal for all species. However, Fig. 3 suggests that this is not the case. Some of the species patterns seem to follow predictions from this hypothesis. Chaffinches and blue tits, the first species to be expected in the smallest woods, are more numerous than other species in the two regions, whereas the black woodpecker, green woodpecker and golden oriole are among the least abundant. The hypothesis of Ambuel & Temple (1983) can only be tested experimentally by manipulation of competitors and predators. However, because the selected woodlots are so small that even their centre is reached by edge species or by predators coming from outside, hypothesis (2) does not offer a plausible explanation of the area effect we found. According to Wright & Hubbell (1983), the extinction rate hypothesis (3) predicts sigmoid incidence curves. Because territories left open by the death of individuals may be filled by offspring as well as by immigrants, differences in fecundity and vagility of species should result in a different likelihood of their presence in equally sized woods not differing in isolation. The sigmoid incidence curves (Fig. 3) suggest that these predictions hold for the woodland birds in the study area. The
348
P. Opdam, G. Rijsdo'k, F. Hustings
immigration rate may affect the duration of the extinction interval, both in small woods, irrespective of isolation, and in remote woods, irrespective of their size. Arrangement of species according to the regression coefficient of area and distance variables (Tables 5 and 6) gives a remarkably similar sequence, which suggests that different immigration rates of species account for the effects of area and distance in a similar way.
TABLE 6 Isolation Effect in Woodland Birds (Partial correlation coefficients for the logistic regression of presence of species on distance from large forest ( D L F ) and area of forest within a 3 km radius (AF3), allowing for variation in woodlot size and habitat differences)
Species
DL F
A F3
Redstart Nuthatch Hawfinch Marsh tit Green woodpecker Great spotted woodpecker Spotted flycatcher Lesser spotted woodpecker Pied flycatcher Tree creeper
--0.94* - 0-80 -0-61" - 0.49 -0.42 -0.39 - 0.23 - 0.14 - 0.25
0.0077* 0.0031"* 0.0037 0.0023* 0.0027 0'0005 0.0014 0"0018 ° 0.0020 - 0.0003
** p <0-02
* p
°p
That territorial breeding pairs require a minimum area for existence (hypothesis (4)) is obvious. One would expect to find this type of area effect in species with the largest territories, irrespective of the degree of isolation. This is confirmed by the data for the great spotted woodpecker and the tree creeper, showing a significant area effect but no effect of isolation. In sum, our data suggest that the occurrence of species in wooded isolates is governed by the abundance of the species in surrounding forests, the population size in the woodlot, and the minimum patch size of a species habitat.
Small woods as habitat islands./or breeding birds
349
The role of isolation
If death of individuals in small isolated woods is rapidly compensated for by immigration, these individuals are likely to be replaced before the next breeding season, and extinction will not be recorded by breeding bird censuses. With decreasing dispersal rates the interval between extinction and immigration increases and extinction is more likely to be recorded during the breeding season. Since remote islands might be reached less often by trespassers than less isolated woods, low-dispersive species will be absent more often in the remote isolates, whereas for highly dispersive species such differences will not be found. Thus, the sequence of species in Table 6 can be explained by specific dispersal rates. Both distance from large forest area and area of woodland within 3 km radius are good predictors for the isolation effect, but this can be attributed to the fact that they are correlated. An isolation effect on the number of species was only found in the restricted set of 15 species of mature woodland. This would mean that the variation in the total species number attributable to isolation is small, and that the species not included in the final data set are not influenced by distance from other woods. Four of these species (long-tailed tit, blackcap, willow tit, and robin) which were not very widely spread in the woodlots were tested for area and isolation effect. Significant area variables were not found for any of them, and only the occurrence of the long-tailed tit was significantly correlated with area of woodland within a 3 km radius. Are mature woodlots habitat islands for birds?
The present results suggest that in small isolated woods the immigration rates of several species are not high enough to compensate for extinctions within a short time. Immigration rates seem to be affected by distance. Hence, for at least some breeding bird species, isolated woodlots can be regarded as habitat islands. Because most bird species in a woodlot seem to be unaffected by the island effect, MacArthur & Wilson's (1967) dynamic equilibrium theory does not seem to offer an appropriate description of avian community dynamics. Even the species which are affected seem to have different extinction and immigration rates and would therefore have a different likelihood of being present in a particular isolated site. We conclude that
P. Opdam, G. Rijsdijk, F. Hustings
350
our results do not support MacArthur & Wilson's dynamic equilibrium theory, but are consistent with their assumption that in small isolated populations local extinction and immigration are important processes that may influence species distribution.
Applications in landscape planning The presence of a species in a habitat isolate is primarily correlated with habitat attributes such as vegetation structure and plant species composition. However, our results indicate that patch size and isolation significantly influence the distribution of species in a patchy environment. In the modern agricultural landscape, many species find their habitat as scattered isolates in a matrix of unsuitable patches. In fact, the areas studied are fairly representative of this landscape type. Therefore, the results of this study can be extrapolated to other areas in so far as to select wood size and distance to large forest in relation to a preferred composition of the bird fauna. For a given number of bird species, Fig. 4 shows the relation between wood size and distance from nearest large forest area. These size-isolation lines are useful for conservation and Size { h a ) 800. 400200"
oo
50-
0,05 0.I
~/
0,5 I
2
5 10 20
/
50
I00
DLF (km)
Fig. 4. Size-isolation lines showing, for a given n u m b e r of bird species, the relation between woodlot size a n d distance from large forest area ( - - , Gelderse Vallei; .... , Limburg).
Small woods as habitat islandsfor breeding birds
351
planning, e.g. to determine the desirable w o o d l o t size given a fixed degree of isolation and a chosen species number. The predictable sequence of species extinctions with decreasing w o o d l o t size makes it possible roughly to associate species number with species composition. Generalisation of our results to other habitat types is not possible, however. Mature woodland can be regarded as one of the least dynamic habitats in the man-dominated landscape. Birds inhabiting stable habitats are thought to be less dispersive than species in dynamic environments (Wiens, 1976; Andersson, 1980; Mikkonen, 1983).
REFERENCES Alvey, N., Galway, N. & Lane, P. (1982). An introduction to GENSTAT. London, New York, Paris, Academic Press. Ambuel, B. & Temple, S. A. (1983). Area dependent changes in the bird communities and vegetation of southern Wisconsin forests. Ecology, 64, 1057-68. Andersson, H. (1980). Nomadism and site tenacity as alternative reproductive tactics in birds. J. Anim. Ecol., 49, 175-84. Connor, E. F. & McCoy, E. D. (1979). The statistics and biology of the species area relationship. Am. Nat., 113, 791-833. Diamond, J. M. (1975). The island dilemma: lessons of modern biogeographic studies for the design of natural reserves. Biol. Conserv., 7, 129-46. Fritz, R. S. (1979). Consequences of insular population structure: Distribution and extinction of spruce grouse populations. Oecologia, 42, 57-65. Galli, A. E., Leck, C. F. & Forman, R. T. T. (1976). Avian distribution patterns in forest islands of different sizes in central New Jersey. Auk, 93, 356-64. Gilbert, F. S. (1980). The equilibrium theory of island biogeography: Fact or fiction? J. Biogeogr., 7, 209 35. Helliwell, D. R. (1976). The effect of size and isolation on the conservation value of wooded sites in Britain. J. Biogeogr., 3, 407-16. Humphreys, W. F. & Kitchener, D. J. (1982). The effect of habitat utilization on species area curves: Implications for optimal reserve area. J. Biogeogr., 9, 391-6. Hustings, M. F. H., Kwak, R. G. M., Opdam, P. F. M. & Reijnen, M.J.S.M. (1985). Natuurbeheer in Nederland, 3. Vogelinventarisatie. Wageningen, Pudoc. Jones, H. L. & Diamond, J. H. (1976). Short-time-base studies on turnover in breeding bird populations on the California Channel islands. Condor, 78, 526-49. Kwak, R. & Meijer, R. (1985). Interpretatiecriteria voor broedvogelinventarisaties met de territoriumkartering. Limosa, 58, 97-108.
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Lynch, J. F. & Whigham, D. F. (1984). Effects of forest fragmentation on breeding bird communities in Maryland, USA. Biol. Conserv., 28, 287-324. MacArthur, R. H. & Wilson, E. O. (1967). The theory of island biogeography. Princeton, University Press. Margules, C., Higgs, A. J. & Rafe, R. W. (1982). Modern biogeographic theory: Are there any lessons for nature reserve design ? Biol. Conserv., 24, 115-28. Mauriello, D. & Roskoski, J. P. (1974). A re-analysis of Vuilleumier's data. Am. Nat., 108, 711-14. Mikkonen, A. V. (1983). Breeding site tenacity of the chaffinch Fringilla coelebs and the brambling F. montifringilla in northern Finland. Orn. Scand., 14, 36-47. Opdam, P. (1983). Verspreiding van broedvogels in het cultuurlandschap: de betekenis van oppervlakte en isolatie van ecotopen. Mededelingen WLO, 10, 179-89. Opdam, P. & Retel Helmrich, V. (1984). Vogelgemeenschappen van heide en hoogveen: een typologische beschrijving. Limosa, 57, 47-63. Opdam, P., Van Dorp, D. & Ter Braak, C. J. F. (1984). The effect of isolation on the number of woodland birds of small woods in the Netherlands. J. Biogeogr., 11, 473-8. Vuilleumier, F. (1970). Insular biogeography in continental regions, I. The northern Andes of South America. Am. Nat., 104, 373-88. Whitcomb, R. F., Robbins, L. S., Lynch, J. F., Whitcomb, B. L., Klimkiewicz, M. K. & Bystrak, D. (1981). Effects of forest fragmentation on avifauna of the eastern deciduous forest. In Forest island dynamics in man dominated landscapes, ed. by R. L. Burgess and D. M. Sharpe, 125-205. Springer, New York. Wiens, J. A. (1976). Population responses to patchy environments. Annu. Rev. Ecol. Syst., 7, 81-120. Woolhouse, M. E. J. (1983). The theory and practice of the species-area effect, applied to the breeding birds of the British woods. Biol. Conserv., 27, 315-32. Wright, S. J. & Hubbell, S. P. (1983). Stochastic extinction and reserve size: A focal species approach. Oikos, 41, 466-76.
Bird Communities in Small Woods in an Agricultural Landscape: Effects of Area and Isolation P. O p d a m , G. Rijsdijk & F. Hustings Research Institute for Nature Management, PO Box 46, 3956 ZR Leersum, The Netherlands
ABSTRACT The distribution oJ breeding bird species in 68 small woodlots in two areas o] agricultural landscape was investigated. Effects oj area, habitat variation, interpatch distance, and distance j?om extensive woods were analysed with the help oJ multivariate techniques. No correlation was Jound between number of breeding bird species and isolation variables, but the degree of isolation was shown to affect the number oJ bird species restricted to mature woods. Species showed different responses to changes ojarea or isolation variables. It is concluded that,Jor several species of woodland birds, patches of mature woodland can be regarded as habitat islands. Some indications are given to apply the regression modelsjound to landscape planning.
INTRODUCTION The distribution of birds in a patchy environment is determined primarily by the presence of suitable habitat. The size of the habitat patches may, however, affect the presence of species, since patch size is related to population size and thereby to extinction rate (Jones & Diamond, 1976; Wright & Hubbell, 1983). At the same time, the distance between the patches may be inversely related to the frequency of interpatch dispersal (Whitcomb et al., 1981; Opdam, 1983; Lynch & Whigham, 1984). The equilibrium theory of MacArthur & Wilson (1967) combined extinction and immigration rates in a dynamic model for the number of species on oceanic islands, and various authors later extended the 333 Biol. Conserv. 0006-3207/85/$03.30 ,t~ ElsevierApplied SciencePublishersLtd, England, 1985. Printed in Great Britain
334
P. Opdam, G. Rijsdiik, F. Hustings
predictions of the model to habitat patches on the mainland. The empirical support for this theory and the implications for reserve design have been discussed exhaustively (Diamond, 1975; Connor & McCoy, 1979; Gilbert, 1980; Margules et al., 1982). However, evidence supporting an area-dependent extinction rate and a distance-dependent immigration rate is scanty (Gilbert, 1980; Margules et al., 1982). For mobile species, such as most birds, Margules et al. (1982) and Ambuel & Temple (1983) even postulate that isolation of reserves will not affect local immigration. In this paper the distribution of breeding birds is discussed in relation to the size and degree of isolation of wooded patches. It is clear that in the modern cultivated landscape, patches of habitat tend to decrease in size and become more and more widely separated from each other. Quantification of the relation between landscape structure and the distribution and survival of fauna groups is an important task for nature conservationists. We chose birds for the present analysis because they can be censused quickly, and woods because great numbers of birds breed in this type of habitat. Effects of patch size on the number of breeding-bird species have been studied often, but in most of these studies, the effects of size p e r se were not separated from those of habitat diversity increasing with size (Connor & McCoy, 1979, but see Ambuel & Temple, 1983). Furthermore, in most studies the variable "number of species" encompassed all the species of a taxonomic order. However, the study done by Humphreys & Kitchener (1982) indicated, as expected, that species restricted to habitats in isolated patches may show species area relations differing strongly from those of species that use adjacent habitats as well, and Galli et al. (1976), Whitcomb et al. (1981) and Opdam & Retel Helmrich (1984) have also pointed to species-specific relations with patch size. The impact of isolation on birds in habitat patches is not quite clear. An effect has been claimed by Fritz (1979), Whitcomb et al. (1981) and Opdam et al. (1984). In the first-mentioned study the spruce grouse C a n a c h i t e s canadensis was shown to occupy habitat remnants more often the closer these patches were to another patch. In the other studies, large sets of data were used to analyse the island effect of small woods on the number of breeding birds. However, the results of Whitcomb et al. (1981) were not unambiguous because in their data wood area and degree of isolation were strongly interdependant, whereas Opdam et al. (1984) could not account for possible habitat variation affecting the distribution
Small woods as habitat islands".[or breeding birds
335
of bird species. In a study on bird-species numbers in British woods, Helliwell (1976) found no effect of isolation, probfibly because he had included in the analysis too m a n y species for which the woods did not represent isolated habitat patches. In Vuilleumier's (1970) analysis of birds on mountain tops the number of species was even positively correlated with distance, but after re-examination of the data Mauriello & Roskoski (1974) claimed that the coefficient of distance should have been negative. The results of the studies done so far are not very convincing, the more so because differences between species were not quantified. In a recent paper, however, Lynch & Whigham (1984) presented an excellent analysis of the avian communities of 185 forest patches ranging in size from 5 to more than 1000 ha and divided over two regions. They could demonstrate the impact of isolation on the distribution of most of the species they studied. In our study we followed more or less the same strategy and selected in an agricultural landscape 68 small woodlots, ranging in size from less than 1 ha to 20 ha. The woodlots differed substantially as to degree of isolation, but otherwise we tried to keep habitat characteristics as uniform as possible. The remaining habitat variation was measured. The presence of all breeding bird species was determined and the following predictions were tested: (a)
Woodlot size and degree of isolation affect the number of bird species. (b) Species that are restricted to woods occur less often in small woodlots than in large ones, even after corrections for differences in habitat structure. (c) These species are absent most often in the most isolated woodlots. (d) Species differ as to the degree to which they are affected by area and isolation. METHODS Two study areas were chosen (Fig. 1). One of them, the Gelderse Vallei (Fig. l a), an agricultural area of about 400 km 2 in the central part of The Netherlands, is surrounded on three sides by extensive mixed forests. Many woods, wooded banks, hedgerows and small groups of trees are scattered over the area, but most of the woods are coppice or half-grown. Within this area 40 mature deciduous woods were selected. The second
336
P. Opdam, G. Rijsdijk, F. Hustings
/ / /
o
,/ /
/ /
o &
o
/
• 0
•
~
•
•
sample plots • 0-2, 0ha zx 2, I - 6 , 0 h a o >6, Oha
Fig. I.
--*-- dutch border ~-~
forest
Location of sample sites in (a) the Gelderse Vallei area and (b) the southern part
of the province of Limburg (Zuid Limburg), showing the outline of surrounding forests. (Scale: 1 cm equals 22km).
area is situated in the southernmost part of the province of Limburg and extends over 200 km z. On the north and south, extensive mixed forests border the area. In this agriculturally-used landscape deciduous woods are scattered; among these 28 mature woods were suitable for our study. The Limburg area (Fig. l b) is more open than the Gelderse Vallei, with fewer wooded sites and groups of trees between the selected woods. Although the sampling plots were selected for uniformity of the tree layer, some divergence between the sites had to be accepted. Moreover, the coverage, structural heterogeneity, and species composition of the shrub layer varied considerably. Therefore, habitat diversity variables were recorded in the field (Table 1). Most edges of the woodlots were sharp changes from trees to cultivated fields. From maps 1:25 000, isolation variables were calculated, and a map 1:10 000 was used to estimate the area of the woodlots (Table I). Because oblong woods have a higher edge-to-interior ratio than compact woods and the forest-edge may represent a different habitat type, the woods were
Small woods as habitat islands jor breeding birds
337
TABLE 1
Variables for Habitat and Landscape Attributes Determined for Each Sample Site Habitat variables
Trunk CovH CovS StrDiv
Trunk diameter, a measure of age differences between trees (2 classes) Coverage of the herb layer (3 classes) Coverage of the shrub layer (3 classes) Structural diversity of tree and shrub layers (3 classes) Dominant tree species (9 types)
Variables of size and landscape
SW A TA DLF DW DAW NDW AAW WB
Shape of the woodlot (compact or oblong) Area of mature deciduous wood (in ha) Total area of wood containing the selected site Distance from large forest areas, measured as the shortest distance between the edge of the woodlot and the edge of an extensive forest area Distance from nearest mature deciduous wood larger than 20 ha (in km) Distance from nearest wood of any type larger than 20 ha (in km) Number of mature deciduous woods within a 3 km radius from the centre of the woodlot Area of wood of any type within a 3 km radius from the centre of the woodlot (in ha) Proximity of wooded banks or rows of mature trees
classified as o b l o n g or c o m p a c t . S o m e o f the w o o d l o t attributes a p p e a r e d to be c o r r e l a t e d (Table 2). E a c h w o o d l o t was visited five times, between M a r c h and the middle o f J u n e o f 1983, for periods o f 15 min each. D u r i n g each visit all parts o f the w o o d were scanned for birds showing b e h a v i o u r indicating the presence o f a territory. In the largest w o o d l o t s m o r e time was n e e d e d to cross the whole area, at m o s t between 30 and 45 min. F o r all species, the first relevant o b s e r v a t i o n was r e c o r d e d o n each visit a n d the presence o f a t e r r i t o r y was derived f r o m the c o m b i n e d visits on the basis o f the criteria in Hustings et al. (1985). F o r m o s t s e d e n t a r y species at least two o b s e r v a t i o n s m a d e o n separate visits were required, but for some species for which o b s e r v a t i o n efficiency was low we accepted a t e r r i t o r y on the basis o f o n l y one r e c o r d in the p o s t - m i g r a t i o n period. In this way a list o f b r e e d i n g birds was o b t a i n e d for each w o o d l o t . T h r e e sets o f analyses were carried out: (a) with the n u m b e r o f species restricted to w o o d s ; (b) with the n u m b e r o f species restricted to m a t u r e d e c i d u o u s w o o d s ; a n d (c) with the p r e s e n c e / a b s e n c e o f p a r t i c u l a r species. T h e last o f these variables assumes either 0 or 1, the o t h e r two range f r o m
P. Opdam, G. Rijsdo'k, F. Hustings
338
TABLE Significant
Correlations
between
Woodlot
2
Attributes
pertaining
to Area
and
Isolation
Gelderse Vallei A~ DAW
WB
5°Jo
--
TA
0 . 1 ~o
--
DLF
--
0.10/o
DW NDW
.
AAW
--
1 o/ /O
__
--
0 - 1 o/. /o
A
DAW
WB
TA
DLF
- -
.
. 5 o~
-_
_
.
0.1 ~o .
.
.
. __
__
DW
NDW
AAW
AAW
WB
Limburg A TA
0 . 1 ~o
DLF
--
DW
--
DAW
--
--
1 ~o
NDW
--
--
O' 1 ~o
--
--
AAW
- -
0 . 1 °/o
0 . 1 °.,o
1 ~o
WB
5 ~o
5 O;o
.
A
TA
DLF
a See Table
-1~o O . l ~o
.
. DW
1 ~o
. DAW
NDW
1.
7 to 39 and from 1 to 11, respectively. The variation of these variables in dependence of the other woodlot attributes was analysed by stepwise multiple linear regression using GENSTAT (Alvey et al., 1982). For several variables (e.g. size and most isolation variables) we assumed nonlinearity in their relation to species number and therefore applied logarithmically transformed values.
RESULTS All woodland species combined As a rule, in studies on the island effect island attributes are related to the total number of species on the (habitat) island, excluding species that also use the habitats surrounding the island. Likewise, we excluded those birds feeding mainly on surrounding agricultural land, and studied the island
Small woods as habitat islands JOt breeding birds
339
effect on the remaining species, which we called w o o d l o t species. Since these birds can inhabit different layers, i.e., the g r o u n d layer, the shrub layer, the c a n o p y , or a c o m b i n a t i o n of layers, some of t h e m are not restricted to the type of w o o d under study, but could also occur in nearby or even adjacent plantations, coppices, hedgerows, or gardens. A significant a m o u n t o f variation in the n u m b e r o f w o o d l o t species is explained by w o o d l o t area a n d a variable o f tree-layer diversity t h a t accounts for the c o m b i n a t i o n o f oaks and beeches (Table 3). This habitat variable was strongly correlated with o a k w o o d a n d the presence of large trees. At the 5 ~o level of significance, none of the isolation parameters were selected. Hence, for all species c o m b i n e d , an effect of isolation could not be d e m o n s t r a t e d . P r o b a b l y the isolation effect was too small to be measurable, because, for most of the species in the set, the w o o d s did n o t represent true habitat islands. W o o d l o t size might be partially related to h a b i t a t diversity, especially as to the coverage, structural heterogeneity, a n d species composition in the shrub layer. A l t h o u g h species area relations are generally described in a double TABLE 3
Summary of Stepwise Multiple Regression Analysis, Showing the Best Over All Fits for the Number of Bird Species in the Woodlots (Standard error between brackets) Sw~ = 16.56 + 2.42 In A + 2.53 BO (0-95) (0"75) (1.22) SwL= 19.96 + 5.161n A - 9.27 POP SMG=5"24--0-551n DLF+0.871nA+I.30BO (0.48) (0-20) (0.31) (0-51) S m = 6.00 + 1.611n A - 0.85 D L F - 2.69 P O P - 1.37 BIO (0-33) (0-16) (0.22) (1.06)' (0"63) SM~=4.11+0-96BO+0.941nA-0.731nDNF+I.85WB Sw, All woodlot species S M, Species of mature deciduous woods G, Gelderse Vallei L, Limburg A, Area BIO, birch-oakwood BO, beech-oakwood POP, poplar-alder DLF, Distance from large forest DNF, Distance from the nearest forest larger than 20 ha
V2 = 39.3 R2 = 42.3 V2 = 78.1 R2 = 79-8 Vz=47.2 R2=51.2 V2 = 86.5 R2 = 88.5 V-'=55.3
R2=61.0
340
P. Opdam, G. R(jsdijk, F. Hustings
logarithmic form, we preferred a semi-logarithmic form because the regression on S gave a slightly better fit (R 2 - - 2 9 . 2 against 27.5). Species restricted to mature woods Since we selected mature deciduous woods as habitat islands, isolation might be particularly relevant with respect to species restricted to woodlots of this type. Therefore a selection was made of 15 species that are found as breeding birds particularly in mature woods, at least in the areas under study (Table 4). Most of these species are numerous in the extensive forests surrounding the study areas. The effects of woodlot size and isolation on the number of these species (S ~ were assessed in the two areas separately. The results of the regression analysis (Table 3) show that in both areas woodlot size and distance to a large forest are significantly correlated with species number. Additionally, the regressions included variables for habitat differences. In the Gelderse Vallei beech-oakwood contained more species than pure oak stands, presumably because TABLE 4 Occurrence of Bird Species of Mature Deciduous Woods in the 68 Plots. (Values are numbers of plots in which each species was
recorded) Species
Values
Black woodpecker Drvocopus martius Woodwarbler Phylloscopus sibilatrix Redstart Phoenicurus phoenicurus Golden oriole Oriol,~s oriolus Green woodpecker Picus viridus Pied flycatcher Ficedula hypoleuca Hawfinch Coccothraustes coccothraustes Lesser spotted woodpecker Dendrocopos minor Marsh tit Parus palustris Nuthatch Sitta europaea Great spotted woodpecker Dendrocopos major Spotted flycatcher Muscicapa striata Tree creeper Certhia brachydactyla Blue tit Parus caeruleus Chaffinch Fringilla coelebs
2° 4b 4 5 7 8" 12b 15 ' 29 37 40 54 59 66 66
In the Gelderse Vallei only b In Limburg only
Small woods as habitat islands for breeding birds
341
beeches offer more nesting holes. In the Limburg area two types of wood (poplar-alder and oak-birch) had fewer species than oakwood and beech-oakwood. These types of wood had mainly half-grown trees and presumably offered fewer feeding sites for bark-feeding birds and fewer nesting holes. Again, because of the better fit, we used a linear-dependent rather than a logarithmic-dependent variable. The variable distance to large forest in the Gelderse Vallei regression model could be replaced by a combination of three variables. The total amount of variation accounted for by this more complicated model did not differ much from that with the simple one. Two of these variables are regarded as indicators of isolation (presence of tree rows and wooded banks around the woodlot and amount of woods within a 3 km radius). Shape of wood, the third variable, is considered as a habitat variable. Oblong-shaped woods, which contained fewer species, are affected most by the surrounding environment (e.g. microclimate) and may therefore be less suitable for typical woodland birds. The coefficients of woodlot size did not differ significantly (t-test, t = 1.17) between the two areas. The greater amount of variation explained by this variable in the Limburg area is attributed to its greater range compared to the Gelderse Vallei (Fig. 2). Since the sample of wooded sites was selected on the basis of tree-layer homogeneity, habitat diversity is rather small. None of the habitat variables was correlated with woodlot size. Hence we suggest that most, if not all, of the effect ofwoodlot size is due to the mere effect of area as such. • L i m b u r g : S : 4 , 7 2 ÷ I , 7 2 In A • G e l d e r s e V a l l e i : S=4,57÷1,27 In A
S 20 16
12 •
04-
÷
•
÷
÷
~"
8 •
4,w e ~
•
•
•
eo+
I
-2(0.14ha)
-I(037ha)
I
(1.00ha} I(2,72ha) 2(7.39ha)
I
3'(20.09ha1 4 InA
Fig. 2.
Species-area plot of the two study areas. (Scale: 1 cm equals 22kin).
342
P. Opdam, G. Rijsd(jk, F. Hustings
Distance to large forest has a somewhat greater impact in the Limburg area as compared with the Gelderse Vallei. This isolation variable ranged between 0.1 and 6.5 km in Limburg and between 0.1 and 9.8 km in the Gelderse Vallei. Calculated over the maximal range, the number of bird species diminished from 8 to 4.4 and from 6.5 to 4, respectively, all other variables being constant. However, the difference between the regression coefficients is not statistically significant (t-test, t = 1.01). A difference between the two areas might be due to the greater amount of woodland and rows or groups of trees in the Gelderse Vallei, which might increase the dispersal rate of woodland birds. We conclude that distance from large forest area is a significant factor determining the distribution of birds inhabiting mature deciduous woods.
Analysis of separate species Thus far, the number of species has been used to analyse the island effect in isolated woodlots. The underlying assumption was that all species are equal with respect to the relationship between woodlot area, population size, and extinction rate, as well as the extent to which their dispersal is hampered by interpatch distance. However, differences between species are plausible and may give more insight into the mechanism leading to the observed species-area relations. Therefore, we undertook an analysis at the species level. For this purpose, we used the presence/absence of a species in the woodlots as a dependent variable in logistic regression analysis. This meant, however, that the amount of variation became much smaller, especially for species occurring either in a very few or in almost all woodlots. The best possible solution to this problem was to combine all woodlots, which was acceptable because of the small differences between the two regions as to the effects of area and isolation. The occurrence of the species in the woodlots is shown in Table 4. Species found in less that 10 ~o or more than 90 ~o of the samples were omitted from further analysis. The regression analysis was restricted to simple models, each containing one variable for size of the woodlot, one isolation variable and two habitat variables (oak-beech type and other woodland types). We also added a region variable (a d u m m y variable) to account for possible differences between the two areas under study. Three sets of regressions were run, each with a different isolation variable, namely distance from large forest, amount of woodland within 3 k m radius, and proximity of wooded banks or rows of trees.
Small woods as habitat islands for breeding birds
343
For most of the species none of the habitat variables explained a significant part of the variation, with the exception of the nuthatch and the great spotted woodpecker, which occurred more often in beech oak woodland than in any of the other types. The coefficients for woodlot size are shown in Table 5. The ranking of the species according to these coefficients in the three sets of regressions remains roughly the same, especially if only significant coefficients are considered. This concordance can be seen as support for the reliability of these results. TABLE 5 Area Effect in Woodland Birds (Coefficients of correlation between frequency of occurrence and woodlot size, allowing for isolation and habitat differences. Only significant coefficients (P <0.10) are given. The coefficients were calculated for three sets, using as an isolation measure area of woodland within 3 km radius (1), distance from large wood (2), and proximity of wooded banks and rows of trees (3).)
Species Great spotted woodpecker Tree creeper Redstart Nuthatch Hawfinch Marsh tit Lesser spotted woodpecker
(I) 2-28* 1.57" 2.11 1.10" 0.97* 0.87* 0.70
(2)
(3)
2.42* 1.62" 1.14 1.09" 0.93* 0.90* 0.69
2.21" 1.84" -0.99 1-92 1-02" 0.62
* P smaller than 0.05
The regression coefficients for the isolation variables are presented in Table 6, except for the proximity of wooded banks, which showed very low T values. The probability of occurrence of nuthatch and marsh tit is significantly affected by the two isolation variables used and that of the redstart by the amount of nearby forest only, whereas for the lesser spotted woodpecker the coefficient of this isolation variable was almost significant. The coefficients of the two variables show a positive correlation. A more detailed consideration of the relation between presence/absence of species and woodlot size may shed more light on the causal
N=11
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lesser spotted woodpecker
~lreat
spotted woodpecker
/~_ spotted flycatcher
14
12
17
14
1.I'-2,0 2.1'-3.0 3.1'-6,0 >6.'0 size
~
chaffinch
~ k
(%) I00-
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,
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N=11
14
12
17
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0"1.0 1.1'-20 2.1'-3.0 3,1'-6.0 "6.b size
hawf, nch
.- "''marsh tit*
nuthatch*
/ ~ " ~ - - - - ~ - b I ue tit*
/"2JL_/ /-
/
/
./
/ " // .~. . .. .
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~t~,t ree creeper*
Fig. 3. Incidence curves showing the frequency of occurrence (in % of maximal frequency) according to five classes of wood size (in ha) of ten species restricted to mature deciduous woodland (Gelderse Vallei + Zuid Limburg). *Significantly differing from random distribution (X 2 test, P < 0.05).
50
100
(~)
Small woods as habitat islands for breeding birds
345
mechanism underlying the distribution patterns found. In Fig. 3 the woodlots have been classified according to five size classes, which were chosen such that the woods were more or less evenly distributed over the size classes. The blue tit and chaffinch are absent in only a few of the smallest woods. The incidence curve of the spotted flycatcher suggests an effect of habitat rather than of woodlot size. In the Gelderse Vallei this species was recorded more often in beech-oak woods than in oak woods. The great spotted woodpecker and tree creeper occur in almost all woods exceeding 3ha and 1 ha, respectively, but the woodpecker was not recorded in woodlots smaller than 1 ha. The stagnation in the upward trends in class 3 may be due to lack of suitable habitat. The nuthatch and marsh tit show no clear minimal habitat size: apparently they can live in even the smallest woodlots. Their absence in some of the woods must be due to lack of suitable habitat (cf. distribution of the great spotted woodpecker and tree creeper), to isolation or extinction. The distribution of the lesser spotted woodpecker is difficult to explain, except by referring to its very clumped distribution pattern in the Gelderse Vallei. The hawfinch was not recorded in the Gelderse Vallei woods, though it occurs in considerable numbers in the surrounding extensive forests of the Veluwe and the Utrechtse Heuvelrug. In the remaining woods the distribution is partially explained by an effect of woodlot size. The pied flycatcher is too scarce to draw reliable conclusions from its incidence curve. We conclude that at the species level there is a good evidence for effects ofwoodlot size, especially in the great spotted woodpecker (minimal area) and in the tree creeper, nuthatch, marsh tit, and hawfinch. Isolation of woodlots is a significant factor in the distribution of the nuthatch, marsh tit and probably the redstart and lesser spotted woodpecker. Because the species are affected to different degrees, they show species-specific distribution patterns.
DISCUSSION Evaluation of the bird survey method
Some researchers have been concerned about the influence of sampling methods on species-area relationships. Woolhouse (1983) argued that sampling time per unit area must be constant for all sites surveyed. For a
346
P. Opdam, G. Rijsdijk, F. Hustings
qualitative survey of breeding-bird territories, this would mean for each wood and for each bird species, equal time spent in one territory. Because the position of territories cannot be known in advance, this condition is hardly attainable in practice, if at all. Further problems are associated with the differences in territory size and observing chance between the species and from the fact that isolated territory owners in a small woodlot may be less active in territorial display than birds in territories surrounded by neighbours. Also, one territory out of a cluster of several is more likely to be recorded solely by pure chance than an isolated one is, even if the sampling effort is the same. We attempted to deal with these problems in several ways. In the first place, observation time was held constant in the smallest woods (up to 4-5 ha, depending on the shape). These woods were so small that it was highly probable that any bird singing would be noticed. In the larger woodlots, which were less easy to survey at a glance, observation time was increased, up to 45 min for a 30 ha wood, depending on the time needed to take a quick look at every section of the wood. Thus, sampling effort (time per unit area) was highest in the smallest woodlots, in agreement with the decreased territorial activities of isolated birds and the increasing chance of recording a single specimen with increasing population size. With this method, however, single small territories in large woods were underestimated, and therefore differences between small and large woods may be somewhat underrated. Because in large woods most of the species in question were represented by several breeding pairs, this bias is assumed to be very small. Differences in recording chance between species were accounted for by the species-specific criteria for the number of records (in combination with recording date) required for the acceptance of a territory (Hustings et al., 1985). These criteria were chosen such that all species were surveyed at an accuracy level of at least 90 ~ (Kwak & Meijer, 1985). The role of patch size
Lynch & Whigham (1984) concluded that the occurrence of many species can be predicted better from structural and floristic characteristics of woods than from patch size and isolation. However, in the uniform series of woods we have intentionally chosen, habitat differences play a minor role and the distribution of most bird species, as well as the composition of avian communities, are predicted best from patch size. The incidence
Small woods as habitat islands Jbr breeding birds
347
curves (Fig. 3) indicate that with increasing woodlot size species are added in a fairly predictable sequence. Several explanations can be offered for this pattern: (1) The bird community in a wood is a random sample of that in the nearest larger woods, and with increasing patch size species are added in order of their overall abundance. Species do not differ as to immigration or extinction rate. This 'random sampling hypothesis' does not imply any biological process and can be used as a null hypothesis to test alternative models (Connor & McCoy, 1979). (2) Forest-interior species cannot persist in the smallest woods because of competition with edge species for nest sites or for food, or become extinct as a result of predation by predators from the surrounding landscape (Ambuel & Temple, 1983). (3) In the smallest woods, populations have the highest extinction rates due to stochastic perturbations of the population number (MacArthur & Wilson, 1967). (4) Species differ as to the minimal critical area they need to satisfy their food requirements during the breeding season. The random-sampling hypothesis predicts that the slopes of the incidence curves are equal for all species. However, Fig. 3 suggests that this is not the case. Some of the species patterns seem to follow predictions from this hypothesis. Chaffinches and blue tits, the first species to be expected in the smallest woods, are more numerous than other species in the two regions, whereas the black woodpecker, green woodpecker and golden oriole are among the least abundant. The hypothesis of Ambuel & Temple (1983) can only be tested experimentally by manipulation of competitors and predators. However, because the selected woodlots are so small that even their centre is reached by edge species or by predators coming from outside, hypothesis (2) does not offer a plausible explanation of the area effect we found. According to Wright & Hubbell (1983), the extinction rate hypothesis (3) predicts sigmoid incidence curves. Because territories left open by the death of individuals may be filled by offspring as well as by immigrants, differences in fecundity and vagility of species should result in a different likelihood of their presence in equally sized woods not differing in isolation. The sigmoid incidence curves (Fig. 3) suggest that these predictions hold for the woodland birds in the study area. The
348
P. Opdam, G. Rijsdo'k, F. Hustings
immigration rate may affect the duration of the extinction interval, both in small woods, irrespective of isolation, and in remote woods, irrespective of their size. Arrangement of species according to the regression coefficient of area and distance variables (Tables 5 and 6) gives a remarkably similar sequence, which suggests that different immigration rates of species account for the effects of area and distance in a similar way.
TABLE 6 Isolation Effect in Woodland Birds (Partial correlation coefficients for the logistic regression of presence of species on distance from large forest ( D L F ) and area of forest within a 3 km radius (AF3), allowing for variation in woodlot size and habitat differences)
Species
DL F
A F3
Redstart Nuthatch Hawfinch Marsh tit Green woodpecker Great spotted woodpecker Spotted flycatcher Lesser spotted woodpecker Pied flycatcher Tree creeper
--0.94* - 0-80 -0-61" - 0.49 -0.42 -0.39 - 0.23 - 0.14 - 0.25
0.0077* 0.0031"* 0.0037 0.0023* 0.0027 0'0005 0.0014 0"0018 ° 0.0020 - 0.0003
** p <0-02
* p
°p
That territorial breeding pairs require a minimum area for existence (hypothesis (4)) is obvious. One would expect to find this type of area effect in species with the largest territories, irrespective of the degree of isolation. This is confirmed by the data for the great spotted woodpecker and the tree creeper, showing a significant area effect but no effect of isolation. In sum, our data suggest that the occurrence of species in wooded isolates is governed by the abundance of the species in surrounding forests, the population size in the woodlot, and the minimum patch size of a species habitat.
Small woods as habitat islands./or breeding birds
349
The role of isolation
If death of individuals in small isolated woods is rapidly compensated for by immigration, these individuals are likely to be replaced before the next breeding season, and extinction will not be recorded by breeding bird censuses. With decreasing dispersal rates the interval between extinction and immigration increases and extinction is more likely to be recorded during the breeding season. Since remote islands might be reached less often by trespassers than less isolated woods, low-dispersive species will be absent more often in the remote isolates, whereas for highly dispersive species such differences will not be found. Thus, the sequence of species in Table 6 can be explained by specific dispersal rates. Both distance from large forest area and area of woodland within 3 km radius are good predictors for the isolation effect, but this can be attributed to the fact that they are correlated. An isolation effect on the number of species was only found in the restricted set of 15 species of mature woodland. This would mean that the variation in the total species number attributable to isolation is small, and that the species not included in the final data set are not influenced by distance from other woods. Four of these species (long-tailed tit, blackcap, willow tit, and robin) which were not very widely spread in the woodlots were tested for area and isolation effect. Significant area variables were not found for any of them, and only the occurrence of the long-tailed tit was significantly correlated with area of woodland within a 3 km radius. Are mature woodlots habitat islands for birds?
The present results suggest that in small isolated woods the immigration rates of several species are not high enough to compensate for extinctions within a short time. Immigration rates seem to be affected by distance. Hence, for at least some breeding bird species, isolated woodlots can be regarded as habitat islands. Because most bird species in a woodlot seem to be unaffected by the island effect, MacArthur & Wilson's (1967) dynamic equilibrium theory does not seem to offer an appropriate description of avian community dynamics. Even the species which are affected seem to have different extinction and immigration rates and would therefore have a different likelihood of being present in a particular isolated site. We conclude that
P. Opdam, G. Rijsdijk, F. Hustings
350
our results do not support MacArthur & Wilson's dynamic equilibrium theory, but are consistent with their assumption that in small isolated populations local extinction and immigration are important processes that may influence species distribution.
Applications in landscape planning The presence of a species in a habitat isolate is primarily correlated with habitat attributes such as vegetation structure and plant species composition. However, our results indicate that patch size and isolation significantly influence the distribution of species in a patchy environment. In the modern agricultural landscape, many species find their habitat as scattered isolates in a matrix of unsuitable patches. In fact, the areas studied are fairly representative of this landscape type. Therefore, the results of this study can be extrapolated to other areas in so far as to select wood size and distance to large forest in relation to a preferred composition of the bird fauna. For a given number of bird species, Fig. 4 shows the relation between wood size and distance from nearest large forest area. These size-isolation lines are useful for conservation and Size { h a ) 800. 400200"
oo
50-
0,05 0.I
~/
0,5 I
2
5 10 20
/
50
I00
DLF (km)
Fig. 4. Size-isolation lines showing, for a given n u m b e r of bird species, the relation between woodlot size a n d distance from large forest area ( - - , Gelderse Vallei; .... , Limburg).
Small woods as habitat islandsfor breeding birds
351
planning, e.g. to determine the desirable w o o d l o t size given a fixed degree of isolation and a chosen species number. The predictable sequence of species extinctions with decreasing w o o d l o t size makes it possible roughly to associate species number with species composition. Generalisation of our results to other habitat types is not possible, however. Mature woodland can be regarded as one of the least dynamic habitats in the man-dominated landscape. Birds inhabiting stable habitats are thought to be less dispersive than species in dynamic environments (Wiens, 1976; Andersson, 1980; Mikkonen, 1983).
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Lynch, J. F. & Whigham, D. F. (1984). Effects of forest fragmentation on breeding bird communities in Maryland, USA. Biol. Conserv., 28, 287-324. MacArthur, R. H. & Wilson, E. O. (1967). The theory of island biogeography. Princeton, University Press. Margules, C., Higgs, A. J. & Rafe, R. W. (1982). Modern biogeographic theory: Are there any lessons for nature reserve design ? Biol. Conserv., 24, 115-28. Mauriello, D. & Roskoski, J. P. (1974). A re-analysis of Vuilleumier's data. Am. Nat., 108, 711-14. Mikkonen, A. V. (1983). Breeding site tenacity of the chaffinch Fringilla coelebs and the brambling F. montifringilla in northern Finland. Orn. Scand., 14, 36-47. Opdam, P. (1983). Verspreiding van broedvogels in het cultuurlandschap: de betekenis van oppervlakte en isolatie van ecotopen. Mededelingen WLO, 10, 179-89. Opdam, P. & Retel Helmrich, V. (1984). Vogelgemeenschappen van heide en hoogveen: een typologische beschrijving. Limosa, 57, 47-63. Opdam, P., Van Dorp, D. & Ter Braak, C. J. F. (1984). The effect of isolation on the number of woodland birds of small woods in the Netherlands. J. Biogeogr., 11, 473-8. Vuilleumier, F. (1970). Insular biogeography in continental regions, I. The northern Andes of South America. Am. Nat., 104, 373-88. Whitcomb, R. F., Robbins, L. S., Lynch, J. F., Whitcomb, B. L., Klimkiewicz, M. K. & Bystrak, D. (1981). Effects of forest fragmentation on avifauna of the eastern deciduous forest. In Forest island dynamics in man dominated landscapes, ed. by R. L. Burgess and D. M. Sharpe, 125-205. Springer, New York. Wiens, J. A. (1976). Population responses to patchy environments. Annu. Rev. Ecol. Syst., 7, 81-120. Woolhouse, M. E. J. (1983). The theory and practice of the species-area effect, applied to the breeding birds of the British woods. Biol. Conserv., 27, 315-32. Wright, S. J. & Hubbell, S. P. (1983). Stochastic extinction and reserve size: A focal species approach. Oikos, 41, 466-76.